Suggested citation: HSE Health Protection Surveillance Centre. Salmonella infection in Ireland, 2018. Dublin: HSE HPSC; 2019 © HSE Health Protection Surveillance Centre, 2019. Reproduction is authorised, provided source is acknowledged

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Key Facts

363 salmonellosis cases notified in 2018 (crude incidence rate of 7.6 per 100,000)

Overall increasing trend in salmonellosis since 2014 (40% increase in four years)

More than half of salmonellosis notifications were associated with international travel

Most common serotypes reported were S. Enteritidis and S. Typhimurium (incl.

monophasic Typhimurium), with S. Typhimurium the most prevalent serotype among

cases acquired in Ireland

Increasing incidence of S Enteridis, both travel-associated and domestically acquired

The largest outbreak reported this year was travel-related, and was suspected to be

foodborne

WGS confirmed majority of cases diagnosed in Ireland genetically unrelated to one

another, but enabled case clusters and sporadic cases in Ireland to be recognised as

being part of larger EU incidents

November 2019

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Salmonella infection in Ireland, 2018

Annual Epidemiological Report

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Table of Contents

Background .......................................................................................................................................................... 3

Methods .............................................................................................................................................................. 3

Disease notification ......................................................................................................................................... 3

Typing of Salmonella isolates .......................................................................................................................... 3

Results ................................................................................................................................................................. 4

Salmonellosis ................................................................................................................................................... 4

Overall incidence ............................................................................................................................................. 4

Strain characteristics ....................................................................................................................................... 4

Geographical and age distribution .................................................................................................................. 4

Disease severity ............................................................................................................................................... 5

Animal contact as a risk factor ........................................................................................................................ 6

Foreign travel as a risk factor for salmonellosis in Ireland .............................................................................. 6

Trends .............................................................................................................................................................. 7

Outbreaks and clusters of salmonellosis ......................................................................................................... 9

Typhoid/Paratyphoid: .................................................................................................................................... 10

Discussion .......................................................................................................................................................... 10

Further information available on HPSC website ............................................................................................... 11

Acknowledgements ........................................................................................................................................... 11

Report prepared by: .......................................................................................................................................... 11

References ......................................................................................................................................................... 11

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Background

Salmonellosis typically presents clinically as an acute enterocolitis, with sudden onset of

abdominal pain, diarrhoea, nausea, headache and occasionally vomiting. Fever is almost

always present. Dehydration, especially among vulnerable populations such as infants, the

immunocompromised and the elderly, may be severe. Invasive infection occurs in a

proportion of cases.

The common reservoirs for non-typhoidal Salmonella are the intestinal tract of domestic

and wild animals (including birds), which may result in a variety of foodstuffs, of both animal

and plant origin, becoming contaminated with faecal organisms either directly or indirectly.

Infected food handlers may also act as a source of contamination for foodstuffs. The

organism may also be transmitted through direct contact with infected animals or humans

or faecally contaminated environments. Companion animals are increasingly being reported

as sources of infection, in particular for children.

Typhoid (caused by S. Typhi) and paratyphoid (caused by S. Paratyphi) cause enteric

fever, a severe systemic life threatening condition; when reported in Ireland, these are

almost invariably travel-associated.

Methods

Disease notification

Salmonellosis, typhoid and paratyphoid are notifiable diseases in Ireland under Infectious

Disease Regulations. Consequently, all medical practitioners, including clinical directors of

diagnostic laboratories, are required to notify the regional Medical Officer of Health (MOH)

of all cases of salmonellosis, typhoid or paratyphoid. Notifications are reported using the

Computerised Infectious Disease Reporting system (CIDR) which is described here.

Further information on the process of reporting notifiable infectious diseases is available

here. The case definitions in use in 2018 are available here. For this report, data on notified

cases of salmonellosis reported to CIDR in 2018 were extracted from CIDR as of 27th

September 2019, and data on typhoid and paratyphoid cases were extracted on October 3rd

2019.

Typing of Salmonella isolates

The National Salmonella, Shigella and Listeria Reference Laboratory (NSSLRL) undertake

whole genome sequencing (WGS) on all Salmonella isolates referred from primary

laboratories, enabling antimicrobial sensitivities to be predicted and genetically-related

clusters to be detected.

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Results

Salmonellosis

Overall incidence

During 2018, 363 cases of salmonellosis were notified (349 confirmed and 14 probable).

Overall this corresponds to a crude incidence rate (CIR) of 7.6 per 100,000 population.

Strain characteristics

The NSSLRL analysed 351 human non-typhoidal Salmonella isolates referred for further

typing in 2018.

The top 10 non-typhoidal serotypes identified in 2018 are displayed in Table 1. As usual, S.

Enteritidis (27%) and S. Typhimurium (including monophasic Typhimurium) (31%) were the

most common serotypes.

Table 1: Top ten non-typhoidal Salmonella serovars in Ireland, 2018

Serotype Number of human isolates %

Enteritidis 95 27.1%

Monophasic Typhimurium 53 15.1%

Typhimurium 56 16.0%

Newport 18 5.1%

Agona 9 2.6%

Kentucky 8 2.3%

Infantis 7 2.0%

Stanley 6 1.7%

Branderup 6 1.7%

Virchow 6 1.7%

Other 24.8% Data source: NSSLRL

More detail on the typing of human Salmonella isolates and their resistance to

antimicrobials is reported in the National Salmonella, Shigella & Listeria Reference

Laboratory of Ireland, Annual Report. 1

Geographical and age distribution

The crude incidence rates varied very little by HSE-area, with all except the HSE-NE being

between 5.7 and 8.1 per 100,000 (Figure 1). The elevated rate in the NE was strongly

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influenced by the inclusion of several HSE-NE cases in a travel-associated outbreak

described below.

Similar to earlier years, the highest age-specific incidence rate was in children under 5

years of age (19.3/100,000). This is likely to be influenced by clinicians more readily

seeking clinical samples in that age group. The next highest rate was in the 20-24 years

age group (11.7 per 100,000); the lowest rate this year was in the 15-19 years age group

(2.6 per 100,000).

Figure 1: Annual crude incidence rate per 100,000 by HSE area, Ireland 2018

Data source: CIDR

Disease severity

Diarrhoea was the most common symptom (97%) among notified cases in 2018 (Table 2),

followed by abdominal pain (84%). Bloody diarrhoea occurred among 32% of cases.

Median duration of illness was eight days (range 1-67 days), based on observations for 192

cases. Where recorded, thirty-eight per cent of cases (135/358) were hospitalised.

Table 2: Disease severity of notified Salmonella cases in Ireland, 2018

Symptom/disease feature

Number with symptom

Number without symptom

Number symptom unknown

Percentage of cases with symptom (among known)

Diarrhoea 323 11 29 97%

Bloody diarrhoea 94 204 65 32%

Vomiting 135 174 54 44%

Nausea 171 93 99 65%

Abdominal pain 241 47 75 84%

Fever 228 63 72 78%

Headache 91 129 143 41%

Myalgia 65 140 158 32% Data source: CIDR

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Animal contact as a risk factor

Contact with pets (e.g. reptiles), with pet food (e.g. frozen rodents, pig ear treats), with

wildlife (e.g. hedgehogs), and with cattle, have all been associated with an increased risk of

salmonellosis. Where recorded on CIDR, 32% (97/307) of salmonellosis cases reported

contact with pets (four of which were reptiles), 9% (25/288) reported contact with farm

animals, 3% (7/202) reported contact with wildlife, and 14% (32/235) reported contact with

pet feed (none with frozen feeder rodents or pig ear treats).

Foreign travel as a risk factor for salmonellosis in Ireland

Where country of infection was reported, 51% (166/328) of cases were travel-associated.

Travel-associated cases peaked between July and October coinciding with the peak

summer holiday period. The seasonal variation among domestically acquired cases was

less pronounced (data not shown).

Among travel associated cases (n=166), the most common countries of infection reported

were Spain (n=31), Bosnia & Herzegovina (n=27), Thailand (n=13), and India (n=10). The

popularity of a country as a travel destination is likely to be an important factor in

determining the number of cases associated with each country. In 2018 the atypically high

number of notifications linked with travel to Bosnia & Herzegovina represent an outbreak.

Table 3: Salmonellosis notifications acquired in Ireland, Europe and Rest of the World by age

group, serotype and quarter, 2018

Characteristic Ireland Europe Rest of the

world

Unknown /Not

Specified Total

Age group

<15 yrs 56 10 16 14 96

15-44 yrs 57 23 46 13 139

45-64 yrs 23 24 19 6 72

65+ yrs 26 24 3 2 55

Serotype

Typhimurium 33 12 6 6 57

Monophasic Typhimurium 25 14 7 2 48

Enteritidis 34 32 16 6 88

Other 62 14 51 11 138

Not specified* 8 10 4 10 32

Quarter

Q1 26 2 9 5 42

Q2 40 11 22 4 77

Q3 51 50 36 12 149

Q4 45 19 17 14 95

Total 162 82 84 35 363 Data source: CIDR *includes 14 probable cases and 18 notifications for which this variable was not completed

Disease acquired in Ireland was more commonly caused by S. Typhimurium and

monophasic Typhimurium strains (38%) than by S. Enteritidis strains (22%), with other

strains making up the remaining 40% of cases (Table 3). By contrast, disease acquired in

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Europe was most commonly associated with S. Enteritidis (44%), followed this year by S.

Typhimurium (incl. monophasic Typhimurium) strains (36%), with other strains accounting

for 19% of cases. For cases associated with acquisition in the Rest of the World, non-

Enteritidis, non-Typhimurium cases predominated (64%), with S. Enteritidis accounting for

20% and S. Typhimurium (incl. monophasic Typhimurium) strains accounting for 23% of

cases (Table 3).

Trends

The 363 cases notified in 2018 represent a 12% decrease compared to 2017; when only

confirmed cases are compared, the 349 cases in 2018 represent an 8% decrease on the

number in 2017 (Figure 2). Overall, notifications have increased 40% from a low of 260

cases notified in 2014, but remain well below levels notified in 2007-2008..

Figure 2: Annual number of notifications and crude incidence rate per 100,000, Ireland 2004-2018

Data source: CIDR

The increase in notifications since 2014 is more pronounced among travel-associated

cases (up 113%), with a more modest increase of 22% among domestically-acquired cases

(Figure 3).

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Figure 3: Salmonellosis notifications by year of notification and travel-status, 2010-2018

Data source: CIDR

Figure 4 shows the distribution of serotypes identified by NSSLRL over the period 2000-

2018. Compared to 2017, the number of cases due to S. Enteritidis increased by 14%, S.

Typhimurium remained similar (up 2%), while those due to other serotypes decreased by

22%. The increasing trend in S. Enteritidis cases since 2014 is observed among both

domestically-acquired and travel-associated notifications (Figure 5).

Figure 4: Annual number of non-typhoidal Salmonella isolates referred to NSSLRL by serotype in Ireland, 2000-2018

Data source: NSSLRL data

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Typhimurium (inc. monophasic) Enteritidis Other serotype

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Figure 5: Annual number of S. Enteritidis isolates by country of infection and year, 2008-2018

Data source: CIDR

Outbreaks and clusters of salmonellosis

During 2018, two general outbreaks and three family outbreaks of salmonellosis were

notified. The largest was an international outbreak of Salmonella monophasic Typhimurium,

sequence type 19 identified initially by the HSE NE among members of a pilgrimage group

returning from Medjugorje, Bosnia and Herzegovina in September 2018. 2 Further cases of

salmonellosis in travellers returning from Medjugorje were reported from five other HSE-

areas, and from another EU Member State, indicating this was a wider event. In total 29

outbreak cases were identified among Irish residents; 18 (62%) of whom were laboratory-

confirmed. The source was not identified, but a continuing foodborne source was suspected

given the distribution of cases over a one month period.2

The second largest outbreak notified was a foodborne family outbreak in the HSE-E with

seven reported ill; a family meal was the suspected vehicle of transmission.

The three remaining outbreaks were small in size (2-3 cases each); two were suspected

foodborne travel-related outbreaks and person-to-person transmission was reported for the

remaining outbreak.

While WGS at NSSLRL has confirmed that the majority of non-typhoidal Salmonella

isolates are not genetically linked, a further 24 non-typhoidal salmonella genetic clusters

were identified by NSSLRL in 2018 in addition to the five notified outbreaks. The median

number of cases in these clusters was two, and cases in eleven of these clusters reported

foreign travel.1,3,4 Many clusters were too diffuse geographically or temporally to require

further public health action. However, one cluster of six cases of S. Enteritidis in 2018 was

genetically linked to a salmonellosis outbreak at European level associated with Polish

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eggs.4 In addition, two apparently sporadic salmonellosis cases were genetically linked to

other international outbreaks identified in Europe.4,5

Typhoid/Paratyphoid:

In 2018, eleven cases of typhoid were notified. Eight were associated with travel to Asia,

principally Pakistan (n=3), India (n=2), and Bangladesh (n=2), one was associated with

Africa. Country of infection was not specified for one case. Six cases occurred in children

aged 15 years or less.

Five paratyphoid cases were notified; all were adults and all were associated with travel to

India.

Discussion

The overall incidence of salmonellosis in Ireland remains low compared to other parts of

Europe.5 Although the CIR reported in 2018 decreased slightly compared to 2017, there

was a large outbreak in 2017 which temporarily elevated the rate, and the rate in 2018 is

consistent with an overall increasing trend since 2014.

The occurrence of travel-associated cases of salmonellosis remains a large contributor to

the overall burden of salmonellosis in Ireland, in particular in summer months. This year, for

the first time, the number of travel acquired salmonellosis cases exceeded the number of

domestically acquired cases, coinciding with increasing foreign travel among Irish residents

as the economic recession recedes.

Because a high proportion of Irish salmonellosis cases are travel-related, they can appear

to be sporadic when viewed in isolation in the Irish dataset. However, WGS has enabled

some travel-associated Irish cases to be linked with outbreaks at European level.3,4

Collaboration with European colleagues is key for identifying and solving such

internationally distributed outbreaks.

Between 2009 and 2014, the number of S. Enteritidis cases was much lower than the

number of S Typhimurium cases, but in recent years, there has been an increasing number

of infections due S. Enteritidis reported such that now they almost match the number

reported for S. Typhimurium. The increase in S. Enteritidis was observed among both

domestically-acquired and travel-associated infections.

Food remains an important transmission route for salmonellosis. Eggs and egg products’

were a significant source of human infection due to Salmonella in Europe and accounted for

over a third of outbreaks reported to the European Food Safety Authority for 2017.6 Various

meat and meat products, and bakery products accounted for another one third of outbreaks

between them at European level. 6 In the United States in 2019, foodborne salmonellosis

outbreaks have been associated with tahini, pre-cut melon, papayas, and minced turkey. 7

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Contact with pets (e.g. reptiles), with pet food (e.g. frozen rodents), with wildlife (e.g.

hedgehogs), and with cattle, have all been associated with an increased risk of

salmonellosis. In the United States in 2019, pig ear dog treats, contact with pet hedgehogs,

and chicks and ducks kept as pets have been implicated in outbreaks. 7 In the UK, frozen

mice produced as feed for pet reptiles have also been reported as a source of

salmonellosis in humans. 8

Further information available on HPSC website

Further information about salmonellosis is available at https://www.hpsc.ie/a-

z/gastroenteric/salmonellosis/

Publications on salmonellosis in Ireland available at https://www.hpsc.ie/a-

z/gastroenteric/salmonellosis/publications/

Acknowledgements

Sincere thanks are extended to all those who participated in the collection of data used in

this report. This includes the notifying physicians, public health doctors, surveillance

scientists, microbiologists, nurses, laboratory staff (in particular the NSSLRL) and

administrative staff.

Report prepared by:

Patricia Garvey and Lois O’Connor

References

1. National Salmonella Shigella & Listeria Reference Laboratory of Ireland, Annual Reports. Available at:

http://www.saolta.ie/documents/

2. Naomi Petty-Saphon, Ian Quintyne, Paul McKeown, Patricia Garvey, John Cuddihy. 2019. An

International Outbreak of Salmonellosis Associated with Travel to Medjugorje Oral Abstract One

Health EJP ASM Dublin, 2019.

https://docs.wixstatic.com/ugd/c416fd_ab7cf6709f424a0ca26b4f1c3cd73b22.pdf

3. Pijnacker et al. 2019. Outbreak of Salmonella enterica serotype Enteritidis linked to eggs from

Poland: a microbiological and epidemiological study. Lancet Infect Dis. 2019 Jul;19(7):778-786. doi:

10.1016/S1473-3099(19)30047-7. Epub 2019 May 24.

4. Patricia Garvey, Niall DeLappe, Mark MaGuire, Joanne King, Paul McKeown, Martin Cormican. 2019.

The Added Value of Routine Whole Genome Sequencing to Public Health Investigation of

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Salmonellosis in Ireland, 2017-2018 Poster abstract One Health EJP ASM Dublin, 2019

https://docs.wixstatic.com/ugd/c416fd_ab7cf6709f424a0ca26b4f1c3cd73b22.pdf

5. European Centre for Disease Prevention and Control/European Food Safety Authority. 2018. Multi-

country outbreak of Salmonella Agona possibly linked to ready-to-eat food – 26 July 2018.

Stockholm and Parma: ECDC/EFSA; 2018.

6. European Food Safety Authority (EFSA), European Centre for Disease Prevention and Control (ECDC).

The Community summary report on trends and sources of zoonoses, zoonotic agents and food-

borne outbreaks in the European Union in 2017. Available at:

https://efsa.onlinelibrary.wiley.com/doi/epdf/10.2903/j.efsa.2018.5500

7. CDC. 2019. Reports of Active Salmonella Outbreak Investigations.

https://www.cdc.gov/salmonella/outbreaks-active.html

8. Kanagarajah et al. 2018. Whole genome sequencing reveals an outbreak of Salmonella Enteritidis

associated with reptile feeder mice in the United Kingdom, 2012-2015. Food Microbiol. 2018

May;71:32-38. doi: 10.1016/j.fm.2017.04.005. Epub 2017 Apr 18.